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ORIGINAL PAPER Pharyngeal Pressures During Swallowing Within and Across Three Sessions: Within-Subject Variance and Order Effects Phoebe R. Macrae Daniel J. Myall Richard D. Jones Maggie-Lee Huckabee Received: 6 May 2010 / Accepted: 21 December 2010 Ó Springer Science+Business Media, LLC 2011 Abstract No studies have investigated within-subject variation in measures of pharyngeal pressures during swallowing across sessions. This study aimed to document the variation in pharyngeal pressures both within and across three sessions. Twenty healthy participants were recruited for three sessions. For each session, peak or nadir pressures were recorded from the upper pharynx (sensor 1), mid-pharynx (sensor 2), and upper esophageal sphincter (sensor 3) during saliva and 10-ml water bolus swallows. Variance was larger across sessions than within sessions for sensors 1 and 2 but comparable for sensor 3. For all sensors there was a high correlation between the variance across sessions and within session (r = 0.92, p \ 0.0001). There were no significant order effects of session or of trial at any sensor with estimated order effects less than 2% and the estimated maximum possible change no larger than 5% for trial and no larger than 12% for session. These data offer direction for longitudinal treatment studies in which pharyngeal pressures are an outcome measurement by (1) providing a basis for power calculations, (2) estimating the likely values of any confounding order effects, and (3) providing suggestions for more reliable data analysis. Keywords Swallowing Á Pharyngeal Á Upper esophageal sphincter Á Pressures Á Variance Á Deglutition Á Deglutition disorders Pharyngeal manometry is frequently used to document the changes associated with various swallowing techniques in both healthy [15] and dysphagic participants [6, 7]. These studies have evaluated immediate maneuver effects by comparing the pressure generated for dry swallows with that generated within the same session for maneuver swallows such as the effortful swallow [17], Mendelsohn maneuver [7], supraglottic swallow [1, 6, 7], tongue-hold maneuver [7, 8], and chin-tuck maneuver [7, 8]. Changes in pressure have also been evaluated for differing bolus sizes [4, 9]. For these studies, it is assumed that within-session manometric measures are reliable and repeatable provided various maneuver swallows are counterbalanced and catheter placement remains stable throughout the session. The reliability of pharyngeal pressure measures obtained over separate sessions is not known. One study has reported acquisition of pharyngeal pressures over two sessions but the researchers normalized the data to account for potential intersession variability [3]. Intersession vari- ability could potentially result from discrepancies in cath- eter position in the pharynx from placement to placement. A study designed to assess the position of a pharyngeal manometric catheter in the pharynx, when placed in one Presented at the 18th Annual Meeting of the Dysphagia Research Society, San Diego, CA, March 2010. P. R. Macrae Á R. D. Jones Á M.-L. Huckabee Department of Communication Disorders, University of Canterbury, Christchurch, New Zealand P. R. Macrae (&) Á D. J. Myall Á R. D. Jones Á M.-L. Huckabee Van der Veer Institute for Parkinson’s and Brain Research, 66 Stewart Street, Christchurch 8011, New Zealand e-mail: [email protected] R. D. Jones Department of Medicine, University of Otago, Christchurch, New Zealand R. D. Jones Department of Medical Physics and Bioengineering, Canterbury District Health Board, Christchurch, New Zealand 123 Dysphagia DOI 10.1007/s00455-010-9324-y

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ORIGINAL PAPER

Pharyngeal Pressures During Swallowing Within and AcrossThree Sessions: Within-Subject Variance and Order Effects

Phoebe R. Macrae • Daniel J. Myall •

Richard D. Jones • Maggie-Lee Huckabee

Received: 6 May 2010 / Accepted: 21 December 2010

� Springer Science+Business Media, LLC 2011

Abstract No studies have investigated within-subject

variation in measures of pharyngeal pressures during

swallowing across sessions. This study aimed to document

the variation in pharyngeal pressures both within and

across three sessions. Twenty healthy participants were

recruited for three sessions. For each session, peak or nadir

pressures were recorded from the upper pharynx (sensor 1),

mid-pharynx (sensor 2), and upper esophageal sphincter

(sensor 3) during saliva and 10-ml water bolus swallows.

Variance was larger across sessions than within sessions

for sensors 1 and 2 but comparable for sensor 3. For all

sensors there was a high correlation between the variance

across sessions and within session (r = 0.92, p \ 0.0001).

There were no significant order effects of session or of trial

at any sensor with estimated order effects less than 2% and

the estimated maximum possible change no larger than 5%

for trial and no larger than 12% for session. These data

offer direction for longitudinal treatment studies in which

pharyngeal pressures are an outcome measurement by (1)

providing a basis for power calculations, (2) estimating the

likely values of any confounding order effects, and (3)

providing suggestions for more reliable data analysis.

Keywords Swallowing � Pharyngeal � Upper esophageal

sphincter � Pressures � Variance � Deglutition � Deglutition

disorders

Pharyngeal manometry is frequently used to document the

changes associated with various swallowing techniques in

both healthy [1–5] and dysphagic participants [6, 7]. These

studies have evaluated immediate maneuver effects by

comparing the pressure generated for dry swallows with

that generated within the same session for maneuver

swallows such as the effortful swallow [1–7], Mendelsohn

maneuver [7], supraglottic swallow [1, 6, 7], tongue-hold

maneuver [7, 8], and chin-tuck maneuver [7, 8]. Changes in

pressure have also been evaluated for differing bolus sizes

[4, 9]. For these studies, it is assumed that within-session

manometric measures are reliable and repeatable provided

various maneuver swallows are counterbalanced and

catheter placement remains stable throughout the session.

The reliability of pharyngeal pressure measures obtained

over separate sessions is not known. One study has

reported acquisition of pharyngeal pressures over two

sessions but the researchers normalized the data to account

for potential intersession variability [3]. Intersession vari-

ability could potentially result from discrepancies in cath-

eter position in the pharynx from placement to placement.

A study designed to assess the position of a pharyngeal

manometric catheter in the pharynx, when placed in one

Presented at the 18th Annual Meeting of the Dysphagia Research

Society, San Diego, CA, March 2010.

P. R. Macrae � R. D. Jones � M.-L. Huckabee

Department of Communication Disorders,

University of Canterbury, Christchurch, New Zealand

P. R. Macrae (&) � D. J. Myall � R. D. Jones � M.-L. Huckabee

Van der Veer Institute for Parkinson’s and Brain Research,

66 Stewart Street, Christchurch 8011, New Zealand

e-mail: [email protected]

R. D. Jones

Department of Medicine, University of Otago, Christchurch,

New Zealand

R. D. Jones

Department of Medical Physics and Bioengineering,

Canterbury District Health Board, Christchurch, New Zealand

123

Dysphagia

DOI 10.1007/s00455-010-9324-y

Page 2: 0595

naris and then the other, found the catheter to sit at midline

for both placements in only one of ten participants [10].

Furthermore, this study found that in some cases lateral

position of the catheter is dependent on the naris in which

the catheter is inserted.

Treatment studies that utilize manometry as an outcome

measure to document changes in pharyngeal pressure

require assurance of measurement stability to attribute any

changes to treatment. No studies have investigated the

variation that results from simply removing and replacing a

manometric catheter in a participant’s pharynx.

The aim of this study was to document the variation in

pharyngeal manometric measures across swallows within

the same session and across three sessions. These data

provide information on the variance introduced into pha-

ryngeal pressure measures as a function of catheter place-

ment, thus allowing for elucidation of treatment effects

from methodological error in rehabilitation studies using

normal participants, and a reference by which to evaluate

the variance in dysphagic participants.

Methods

Participants

Twenty healthy participants (gender equally represented,

age range 18–35 years) were recruited for this study. They

reported no history of dysphagia or neurological impair-

ment. Ethical approval was obtained from the local insti-

tutional review board. Informed consent was obtained prior

to commencement of data collection.

Instrumentation

A 100-cm-long round catheter, 2.1 mm in diameter (Model

CTS3 ? EMG, Gaeltec, Hackensack, NJ), was used for

manometric data collection. The catheter houses three

solid-state, unidirectional, posteriorly oriented sensors

(2 9 5 mm), with 20 mm between sensors 1 and 2 and

30 mm between sensors 2 and 3 (as recommended in [11]).

Data were collected using the Kay Elemetrics Digital

Swallowing Workstation (Kay Elemetrics, Lincoln Park,

NJ). Digitized 12-bit samples were obtained with a sam-

pling frequency of 500 Hz and displayed in a -100 to

500-mmHg display window. The system software gener-

ates pressure waveforms as a function of time. The catheter

was calibrated at 250 mmHg at room temperature. All

measurements were displayed on a computer monitor

during data collection and digitally recorded for offline

analysis.

Procedures

Participants were seated upright in a dental chair. Each

participant completed three sessions, with a wide range of

intersession intervals (from 30 min to 7 days) to minimize

possible bias introduced by a single fixed interval. For

session 1, the lubricated intraluminal catheter was inserted

into one naris. Once the tip of the catheter reached the

upper pharynx, identified by resistance at the posterior

pharyngeal wall, the participant ingested water rapidly

through a straw until the catheter was pulled down

approximately 35 cm into the proximal esophagus. The

catheter was then pulled back out at increments of 10 mm,

until high pressure in sensor 1, the uppermost sensor,

suggested placement in the high-pressure zone of the

cricopharyngeus muscle [12]. Pull-through was then done

in 5-mm increments, requiring the participant to sit sta-

tionary and dry swallow once after a period of approxi-

mately 30 s at each increment. Pull-through was continued

until correct catheter placement was confirmed through

visualization of the typical ‘‘M’’ wave displayed at sensor 3

during swallowing [12]. Standardization of catheter

placement using the M wave has been documented in

numerous studies [2, 3, 5, 9]. Presence of the M wave

indicates placement of the third sensor at the proximal

border of the high-pressure zone of the cricopharyngeus

muscle [12]. UES measures made with the manometry

sensor in this position have been documented to most

closely reflect UES measures made using videofluoroscopy

[13]. Sensors were oriented toward the posterior pharyn-

geal wall [2, 3], as confirmed by continuous monitoring of

unidirectional markers on the catheter. The catheter was

then secured to the nose with medical tape. Sensor 1 was

therefore located in the upper pharynx (approximately even

with the base of the tongue), sensor 2 in the midpharynx

(approximately even with the laryngeal additus), and sen-

sor 3 in the proximal aspect of the tonically contracted UES

[14]. The distance from the third sensor to the nose tip for

session 1 was noted. For sessions 2 and 3, the catheter was

inserted into the same naris and to the same distance in

millimeters from the tip of the nose as was determined

optimal in session 1. Participants executed five dry swal-

lows and five 10-ml water bolus swallows in each session.

A 10-ml water bolus was chosen to provide a contrast in

volume to that of saliva swallows, which can be as much as

2 ml [15]. There is also evidence to suggest that bolus

volume may reach up to 10–12 ml during natural drinking

situations [16]. Participants were prompted to swallow

whenever they felt comfortable, following a 30-s rest

period. Participants were seated so they were unable to

view the waveforms displayed on the computer monitor.

P. R. Macrae et al.: Within-Subject Variance in Pharyngeal Pressures During Swallowing

123

Page 3: 0595

Data Analysis

Peak or nadir pressures for each sensor were obtained

offline. These were defined as the highest (sensors 1 and 2)

or lowest (sensor 3) recorded pressure during each swal-

lowing event. Due to the open cavity formation of the

pharynx, contact pressure recordings were relative to

atmospheric pressure. As one of the two conditions eval-

uated in this study did not involve ingestion of a bolus and

as simultaneous fluoroscopy was not performed, pressure

measurements reflected contact pressure rather than intra-

bolus pressure. Contact pressure represents convergence of

the pharyngeal walls or the functional peristaltic wave of

the pharynx [17].

Statistical Analysis

Using the R statistical analysis environment [18], mixed-

effects models [19, 20] were used to estimate the order effects

and variability of the measures (both between sessions and

within a session). Confidence intervals were calculated for

both the order effects and the variability to indicate the degree

of uncertainty in the estimation of the parameters.

Results

Estimated baseline pressures (in mmHg with 95% confi-

dence intervals) for dry swallows were 95 (77–113), 114

Session and trial

Pre

ssur

e as

a fr

actio

n of

the

rang

e fo

r a

sens

or

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

0.0

0.2

0.4

0.6

0.8

1.0

0.01956

0.04376

0.04739

0.05566

0.07807

1 2 3

0.03756

0.04378

0.04893

0.05644

0.09262

1 2 3

0.03982

0.04394

0.04907

0.06040

0.09746

1 2 3

0.04182

0.04646

0.05041

0.06353

0.14154

1 2 3

variableSensor 1

Sensor 2

Sensor 3

Fig. 1 Individual values for

each of the five dry swallow

trials at each sensor for sessions

1, 2, and 3, for all 20

participants. Values have been

normalized to the range of

values at each sensor, to make

each value a percentage of the

range. Each plot is titled with

the individual mean of within-

session variance and progresses

from least variable to most

variable

P. R. Macrae et al.: Within-Subject Variance in Pharyngeal Pressures During Swallowing

123

Page 4: 0595

(93–136), and -13 (-16 to -10) for sensors 1, 2, and 3,

respectively, and for 10-ml swallows they were 91

(70–112), 112 (90–133), and -8 (-11 to -5). Figure 1 dis-

plays individual values for all 20 participants for each of

the five trials plotted across each session for all three

sensors for dry swallows only, as dry swallows are repre-

sentative of both swallow types.

The variability within and across sessions is shown

in Table 1 as standard deviations with 95% confidence

intervals. Variability is greater across sessions than within

sessions for sensors 1 and 2 during both dry and 10-ml

swallows. The across-session variance measured at sensor

3 is relatively comparable to that measured within sessions.

There were no significant effects of trial or session at any

of the sensors for both dry and 10-ml swallows, with the

estimated maximum change no larger than 5% for trial and

no larger than 12% for session (Table 1).

To examine the relationship between within-session and

across-session variability, correlations of the two were

completed (Fig. 2). An individual’s maximum within-ses-

sion variance was plotted against the standard deviation for

the three sessions for that individual. The two were highly

correlated (r = 0.92, p \ 0.0001), with no difference

between the correlations for any of the three sensors.

Finally, an analysis was completed to probe the influ-

ence of identifying and deleting outliers from the data set.

From visual inspection of Fig. 1, sessions with a standard

deviation of approximately 20% or greater appeared to be

outliers in terms of session variance. Variance at this level

is proposed to reflect participant and/or catheter placement

issues based on the fact that stable measures could be

obtained for the same sensor in another session and/or a

different sensor in the same session. The complete data set

contains 20 participants, three sessions, three sensors, and

two conditions (dry and 10-ml swallows) totaling 360

participant-sensor-condition units. Ten of these units had a

within-session standard deviation greater than 20% and

were excluded to assess the effect of removing invalid

measures, leaving 350 participant-sensor-condition units.

Excluding these units reduced the confidence intervals

around value estimates; for example, at sensor 1 during

10-ml swallows, the initial 95% confidence interval for

the change over sessions of [-8.5 to 10.9] was reduced to

[-5.1 to 7.0], a decrease of 40%.

Discussion

This methodological study is the first to have determined

the within- and across-session variability of pharyngeal

contact pressure recordings during swallowing in normal

subjects. This information is important to the emergence of

manometry as a viable outcome measure in rehabilitation

research. The data presented here represent group vari-

ance for pharyngeal and UES pressures during normal

swallowing physiology and have relevance in interpreting

normative data of pharyngeal pressures provided by pre-

vious studies. Documenting this variance is important for

studies using healthy participants which investigate chan-

ges in pharyngeal function as a result of swallowing

maneuvers. These data are also important for formulating

power calculations for such studies, and for providing a

reference by which to compare dysphagic pharyngeal

pressure variation. These data suggest that peak and nadir

pressures change less than 2% due to order effects, with the

estimated maximal change not likely more than 5% in

consecutive trials and not more than 12% in consecutive

sessions. The data also suggest that for sensors 1 and 2,

variability is greater across sessions than within sessions.

Given the increased variability across sessions compared

with within a session, these data are important to consider

when using manometry for repeated measures to document

change as a result of treatments. The within-session vari-

ance documented here may also be useful for studies

wishing to compare the pressure generation associated

with different swallow techniques in the same session. As

Table 1 Within- and across-session variability in pharyngeal pressures along with estimated order effects for pharyngeal pressures

Swallow Sensor SD across trials

(mmHg)

Estimated change per

trial (mmHg)

SD across sessions

(mmHg)

Estimated change

per session (mmHg)

Dry 1 13.4 (12.2–14.8) 0.4 (-1.2 to 2.0) 18.5 (14.5–23.7) 1.0 (-5.2 to 7.2)

Dry 2 17.3 (15.8–18.9) -0.5 (-1.9 to 0.9) 27.5 (21.7–35.0) -1.0 (-10.1 to 8.2)

Dry 3 3.0 (2.8–3.3) -0.1 (-0.5 to 0.2) 3.6 (2.8–4.7) -0.3 (-1.5 to 1.0)

10-ml 1 16.3 (14.8–17.9) 1.6 (-0.5 to 3.6) 29.4 (23.2–37.2) 1.2 (-8.5 to 10.9)a

10-ml 2 17.7 (16.1–19.5) -1.6 (-3.3 to 0.1) 23.2 (18.1–29.8) -0.1 (-7.9 to 7.8)

10-ml 3 2.6 (2.4–2.9) -0.1 (-0.4 to 0.1)b 2.8 (2.2–3.7) -0.1 (-1.1 to 0.8)

Estimated values are shown with 95% confidence intervals in bracketsa Greatest change across sessions (12%)b Greatest change across trials (5%)

P. R. Macrae et al.: Within-Subject Variance in Pharyngeal Pressures During Swallowing

123

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intrabolus pressure was not measured, the present findings

are applicable to contact pressure only.

One consideration in manometric evaluation of pha-

ryngeal pressures is the use of unidirectional versus

circumferential sensors. The present study used a 2.1-mm-

diameter round catheter housing unidirectional sensors.

Evidence of radial asymmetry of pharyngeal and UES

pressures suggests that circumferential pressure sensors may

be advantageous over unidirectional sensors [21, 22]. There

is further evidence suggesting an advantage of an ovoid

catheter in negating problems with radial asymmetry

[11, 12]; therefore, consideration of the manometry assem-

bly used in this study is warranted. Although circumferential

sensors alleviate the issue of radial pressure asymmetry, the

increased diameter required to accommodate the sensors

may counteract this advantage when looking at pressures in

the pharynx. Variation in manometric recordings has been

confirmed in relation to an increase in catheter diameter [23],

as well as in response to stress [24], which could arguably

play a role in the tolerance of a larger catheter. In addition,

bolus flow is influenced by catheter diameter [17], suggest-

ing that a smaller-diameter catheter may provide more rep-

resentative pharyngeal pressures related to swallowing.

Previous studies using the same catheter assembly as the

present study have shown consistent measures of pharyngeal

pressure [25]. Furthermore, the present study highlights that

by maintaining sensors in a posterior orientation, pressures

within the UES are relatively stable within and across ses-

sions, with no significant order effects and an estimated

maximum change of no more than 5% across trials and 12%

across sessions for all sensors. There is, however, reasonable

variance in pressures measured at all sensors. Comparing the

variance seen in the present study with that documented

using circumferential sensors would provide insight into

how different catheter placements are affected by radial

asymmetry in the pharynx.

The variance within and across sessions depicted in

Fig. 1 shows a larger variation of values for some sessions

than for others, and for some sensors more than others

within individuals. In order to provide empirical evidence

for dysphagia treatment techniques, outcome measures

need to be sensitive to changes in various swallowing

parameters. The considerable within- and across-session

variability documented in this study suggests that attempts

to validate treatments using pharyngeal manometry require

either substantial effect sizes and/or participant numbers. If

sources of variation can be identified and removed, the

application of results from studies incorporating pharyn-

geal manometry should be improved.

Causes of variation across session may relate to changes

in catheter placement. Doeltgen et al. [10] evaluated vari-

ation in catheter placement using radiographic still images.

In five of ten participants, repeat catheter placement did not

change catheter position in the pharynx. If their finding is

applied to the present study, with 50% of participants

showing varied catheter position in consecutive placements

in the pharynx, our data suggest this variance will likely

Maximum within-session variance

Bet

wee

n-se

ssio

n va

rianc

e

0.00

0.02

0.04

0.06

0.08

0.10

0.12

0.00

0.02

0.04

0.06

0.08

0.10

0.12

0.00

0.02

0.04

0.06

0.08

0.10

0.12

0.05 0.10 0.15 0.20 0.25

Sensor 1

Sensor 2

Sensor 3

swallow

10-ml swallow

Dry swallow

Fig. 2 Scatterplots of the relationship between within- and across-

session variability for sensors 1, 2, and 3. Within-session variability

reflects the largest individual within-session standard deviation.

Across-session variability is the standard deviation of the mean of

the three sessions

P. R. Macrae et al.: Within-Subject Variance in Pharyngeal Pressures During Swallowing

123

Page 6: 0595

contribute to the increased variability seen in pressures

across sessions.

Variability within a participant could be influenced by

individual anatomy. Anatomical variations could predis-

pose measurements to the effects of catheter tolerance or

radial asymmetry. An interaction of differential catheter

placement and anatomical differences may create more

variation for one session and/or sensor compared with

others, as seen for the participant with mean within-session

variance of 0.055 in Fig. 1. Completing a similar investi-

gation using radiographs would further elucidate the

influence of catheter placement and anatomical differences

on the variation within and across sessions.

The highly predictive relationship between within- and

across-session variances suggests that utilizing individual

means of pharyngeal pressures for a given session/sensor

may not be the optimal first step in analysis of such data. If

the goal of the investigation is to reliably document change

in swallowing pressures as a result of intervention, then

assessing the within-session variability for individuals and

excluding high-variability sessions/sensors may result in

more definitive results. While excluding data is typically

not ideal in group analysis, and not generally possible in the

assessment of patients, it may be necessary for the purpose

of effective treatment evaluation. So as to avoid bias,

exclusion of data must be based on the inference that true

values of pharyngeal pressure are not being recorded. Fig-

ure 1 shows that while a given sensor may show substantial

variability for a given session, other sessions show very

reproducible values for the same sensor (see the participant

with mean within-session variance of 0.097, sensor 1,

Fig. 1). If high variability within sessions reflected true

variation inherent in each individual swallow, all sessions

should show similar variability for that sensor. The analysis

completed on a subset of these data showed that by elimi-

nating units (sensors for a given session and swallow type)

that varied more than 20% of the range for that sensor,

confidence intervals around values for that sensor were

substantially improved. By excluding these highly variable

units, it greatly increases the confidence that any change

over sessions is small. For treatment studies, large confi-

dence intervals increase the number of participants required

to accurately determine the effect of a treatment.

This study did not assess a range of bolus sizes, using

only a 10-ml water bolus. Sensor 3, where the lumen sur-

rounding the catheter is much smaller than in the pharynx,

is more likely to be influenced by the presence of a bolus.

However, within- and across-session variances were com-

parable across all sensors, for both dry and 10-ml water

swallows. Comparing the variations within and across

sessions documented in the present study with those of

future studies using circumferential sensors and various

bolus sizes would be of interest.

Provided that the variation reported in this study is

considered in analysis of group treatment effects, pharyn-

geal pressure recorded using manometry can provide a

valuable outcome measure for treatment studies. Because

this study did not assess pharyngeal pressures of patients

with dysphagia, the values here must be considered to

reflect normal swallowing physiology only. A meticulous

approach to validation of dysphagia management tech-

niques often involves initially documenting normal physi-

ology [26]. Therefore, although these findings are not

generalizable to the patient population per se, the data

represent a first step in investigating variability in mano-

metric measures of pharyngeal pressures. These data may

serve as a reference for the variability seen in patient

groups and a basis for analysis of further studies of healthy

participants. These data should also be considered in the

interpretation of normative data for pharyngeal pressures.

The large within- and across-subject variability docu-

mented here suggests that further studies in which this

variability is eliminated are needed to gain a clear under-

standing of treatment effects on pharyngeal pressures

before these treatments are applied to patients, where

variability may be greater.

Acknowledgments The research was conducted during the tenure

of a Postgraduate Scholarship of the New ZealandNeurological

Foundation, awarded to the first author, Phoebe Macrae.

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Phoebe R. Macrae BSLT(Hons)

Daniel J. Myall PhD

Richard D. Jones PhD

Maggie-Lee Huckabee PhD

P. R. Macrae et al.: Within-Subject Variance in Pharyngeal Pressures During Swallowing

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